The Activation of the Mirror Neuron System during Action Observation and Action Execution with Mirror Visual Feedback in Stroke: A Systematic Review

Jack J Q Zhang, Kenneth N K Fong, Nandana Welage, Karen P Y Liu, Jack J Q Zhang, Kenneth N K Fong, Nandana Welage, Karen P Y Liu

Abstract

Objective: To evaluate the concurrent and training effects of action observation (AO) and action execution with mirror visual feedback (MVF) on the activation of the mirror neuron system (MNS) and its relationship with the activation of the motor cortex in stroke individuals.

Methods: A literature search using CINAHL, PubMed, PsycINFO, Medline, Web of Science, and SCOPUS to find relevant studies was performed.

Results: A total of 19 articles were included. Two functional magnetic resonance imaging (fMRI) studies reported that MVF could activate the ipsilesional primary motor cortex as well as the MNS in stroke individuals, whereas two other fMRI studies found that the MNS was not activated by MVF in stroke individuals. Two clinical trials reported that long-term action execution with MVF induced a shift of activation toward the ipsilesional hemisphere. Five fMRI studies showed that AO activated the MNS, of which, three found the activation of movement-related areas. Five electroencephalography (EEG) studies demonstrated that AO or MVF enhanced mu suppression over the sensorimotor cortex.

Conclusions: MVF may contribute to stroke recovery by revising the interhemispheric imbalance caused by stroke due to the activation of the MNS. AO may also promote motor relearning in stroke individuals by activating the MNS and motor cortex.

Figures

Figure 1
Figure 1
Flowchart of literature search.

References

    1. Dobkin B. H. Rehabilitation after stroke. New England Journal of Medicine. 2005;352(16):1677–1684. doi: 10.1056/NEJMcp043511.
    1. Lo A. C., Guarino P. D., Richards L. G., et al. Robot-assisted therapy for long-term upper-limb impairment after stroke. New England Journal of Medicine. 2010;362(19):1772–1783. doi: 10.1056/NEJMoa0911341.
    1. Kwakkel G., Veerbeek J. M., van Wegen E. E. H., Wolf S. L. Constraint-induced movement therapy after stroke. The Lancet Neurology. 2015;14(2):224–234. doi: 10.1016/S1474-4422(14)70160-7.
    1. Laver K. E., George S., Thomas S., Deutsch J. E., Crotty M. Virtual reality for stroke rehabilitation. Cochrane Database of Systematic Reviews. 2015;(2, article CD008349) doi: 10.1002/14651858.CD008349.pub3.
    1. Fan Y. T., Lin K. C., Liu H. L., Wu C. Y., Wai Y. Y., Lee T. H. Neural correlates of motor recovery after robot-assisted stroke rehabilitation: a case series study. Neurocase. 2016;22(5):416–425. doi: 10.1080/13554794.2016.1215469.
    1. Liepert J., Miltner W. H. R., Bauder H., et al. Motor cortex plasticity during constraint-induced movement therapy in stroke patients. Neuroscience Letters. 1998;250(1):5–8. doi: 10.1016/S0304-3940(98)00386-3.
    1. Saleh S., Fluet G., Qiu Q., Merians A., Adamovich S. V., Tunik E. Neural patterns of reorganization after intensive robot-assisted virtual reality therapy and repetitive task practice in patients with chronic stroke. Frontiers in Neurology. 2017;8(452):p. 452. doi: 10.3389/fneur.2017.00452.
    1. Ramachandran V. Plasticity and functional recovery in neurology. Clinical Medicine. 2005;5(4):368–373. doi: 10.7861/clinmedicine.5-4-368.
    1. Rizzolatti G., Craighero L. The mirror-neuron system. Annual Review of Neuroscience. 2004;27(1):169–192. doi: 10.1146/annurev.neuro.27.070203.144230.
    1. Rizzolatti G., Luppino G. The cortical motor system. Neuron. 2001;31(6):889–901. doi: 10.1016/S0896-6273(01)00423-8.
    1. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. Journal of Neurophysiology. 1995;73(6):2608–2611. doi: 10.1152/jn.1995.73.6.2608.
    1. Buccino G., Vogt S., Ritzl A., et al. Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron. 2004;42(2):323–334. doi: 10.1016/S0896-6273(04)00181-3.
    1. Frenkel-Toledo S., Liebermann D. G., Bentin S., Soroker N. Dysfunction of the human mirror neuron system in ideomotor apraxia: evidence from mu suppression. Journal of Cognitive Neuroscience. 2016;28(6):775–791. doi: 10.1162/jocn_a_00936.
    1. Chen W., Ye Q., Ji X., et al. Mirror neuron system based therapy for aphasia rehabilitation. Frontiers in Psychology. 2015;6:p. 1665. doi: 10.3389/fpsyg.2015.01665.
    1. Yuan T. F., Hoff R. Mirror neuron system based therapy for emotional disorders. Medical Hypotheses. 2008;71(5):722–726. doi: 10.1016/j.mehy.2008.07.004.
    1. Perry A., Saunders S. N., Stiso J., et al. Effects of prefrontal cortex damage on emotion understanding: EEG and behavioural evidence. Brain. 2017;140(4):1086–1099. doi: 10.1093/brain/awx031.
    1. Garrison K. A., Winstein C. J., Aziz-Zadeh L. The mirror neuron system: a neural substrate for methods in stroke rehabilitation. Neurorehabilitation and Neural Repair. 2010;24(5):404–412. doi: 10.1177/1545968309354536.
    1. Pineda J. A. Sensorimotor cortex as a critical component of an ‘extended’ mirror neuron system: does it solve the development, correspondence, and control problems in mirroring? Behavioral and Brain Functions. 2008;4(1):p. 47. doi: 10.1186/1744-9081-4-47.
    1. Rizzolatti G., Sinigaglia C. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nature Reviews Neuroscience. 2010;11(4):264–274. doi: 10.1038/nrn2805.
    1. Yuan T. F., Chen W., Shan C., et al. Activity-dependent neurorehabilitation beyond physical trainings: “mental exercise” through mirror neuron activation. CNS & Neurological Disorders - Drug Targets. 2015;14(10):1267–1271. doi: 10.2174/1871527315666151111130956.
    1. Sarasso E., Gemma M., Agosta F., Filippi M., Gatti R. Action observation training to improve motor function recovery: a systematic review. Archives of Physiotherapy. 2015;5(1):p. 14. doi: 10.1186/s40945-015-0013-x.
    1. Ertelt D., Small S., Solodkin A., et al. Action observation has a positive impact on rehabilitation of motor deficits after stroke. NeuroImage. 2007;36:T164–T173. doi: 10.1016/j.neuroimage.2007.03.043.
    1. Altschuler E. L., Wisdom S. B., Stone L., et al. Rehabilitation of hemiparesis after stroke with a mirror. The Lancet. 1999;353(9169):2035–2036. doi: 10.1016/S0140-6736(99)00920-4.
    1. Sugg K., Müller S., Winstein C., Hathorn D., Dempsey A. Does action observation training with immediate physical practice improve hemiparetic upper-limb function in chronic stroke? Neurorehabilitation and Neural Repair. 2015;29(9):807–817. doi: 10.1177/1545968314565512.
    1. Franceschini M., Ceravolo M. G., Agosti M., et al. Clinical relevance of action observation in upper-limb stroke rehabilitation: a possible role in recovery of functional dexterity. A randomized clinical trial. Neurorehabilitation and Neural Repair. 2012;26(5):456–462. doi: 10.1177/1545968311427406.
    1. Cowles T., Clark A., Mares K., Peryer G., Stuck R., Pomeroy V. Observation-to-imitate plus practice could add little to physical therapy benefits within 31 days of stroke: translational randomized controlled trial. Neurorehabilitation and Neural Repair. 2013;27(2):173–182. doi: 10.1177/1545968312452470.
    1. Fu J., Zeng M., Shen F., et al. Effects of action observation therapy on upper extremity function, daily activities and motion evoked potential in cerebral infarction patients. Medicine. 2017;96(42, article e8080) doi: 10.1097/MD.0000000000008080.
    1. Sun Y., Wei W., Luo Z., Gan H., Hu X. Improving motor imagery practice with synchronous action observation in stroke patients. Topics in Stroke Rehabilitation. 2016;23(4):245–253. doi: 10.1080/10749357.2016.1141472.
    1. Caspers S., Zilles K., Laird A. R., Eickhoff S. B. ALE meta-analysis of action observation and imitation in the human brain. NeuroImage. 2010;50(3):1148–1167. doi: 10.1016/j.neuroimage.2009.12.112.
    1. Pomeroy V. M., Clark C. A., Miller J. S. G., Baron J. C., Markus H. S., Tallis R. C. The potential for utilizing the “mirror neurone system” to enhance recovery of the severely affected upper limb early after stroke: a review and hypothesis. Neurorehabilitation and Neural Repair. 2005;19(1):4–13. doi: 10.1177/1545968304274351.
    1. Ramachandran V. S., Altschuler E. L. The use of visual feedback, in particular mirror visual feedback, in restoring brain function. Brain. 2009;132(7):1693–1710. doi: 10.1093/brain/awp135.
    1. Eng K., Siekierka E., Pyk P., et al. Interactive visuo-motor therapy system for stroke rehabilitation. Medical & Biological Engineering & Computing. 2007;45(9):901–907. doi: 10.1007/s11517-007-0239-1.
    1. Toh S. F. M., Fong K. N. K. Systematic review on the effectiveness of mirror therapy in training upper limb hemiparesis after stroke. Hong Kong Journal of Occupational Therapy. 2012;22(2):84–95. doi: 10.1016/j.hkjot.2012.12.009.
    1. Saleh S., Yarossi M., Manuweera T., Adamovich S., Tunik E. Network interactions underlying mirror feedback in stroke: a dynamic causal modeling study. NeuroImage: Clinical. 2017;13:46–54. doi: 10.1016/j.nicl.2016.11.012.
    1. Deconinck F. J. A., Smorenburg A. R. P., Benham A., Ledebt A., Feltham M. G., Savelsbergh G. J. P. Reflections on mirror therapy: a systematic review of the effect of mirror visual feedback on the brain. Neurorehabilitation and Neural Repair. 2015;29(4):349–361. doi: 10.1177/1545968314546134.
    1. Auriat A. M., Neva J. L., Peters S., Ferris J. K., Boyd L. A. A review of transcranial magnetic stimulation and multimodal neuroimaging to characterize post-stroke neuroplasticity. Frontiers in Neurology. 2015;6:p. 226. doi: 10.3389/fneur.2015.00226.
    1. Hobson H. M., Bishop D. V. M. Mu suppression – a good measure of the human mirror neuron system? Cortex. 2016;82:290–310. doi: 10.1016/j.cortex.2016.03.019.
    1. Muthukumaraswamy S. D., Singh K. D. Modulation of the human mirror neuron system during cognitive activity. Psychophysiology. 2008;45(6):896–905. doi: 10.1111/j.1469-8986.2008.00711.x.
    1. Calabrò R. S., Naro A., Russo M., et al. The role of virtual reality in improving motor performance as revealed by EEG: a randomized clinical trial. Journal of NeuroEngineering and Rehabilitation. 2017;14(1):p. 53. doi: 10.1186/s12984-017-0268-4.
    1. Guo F., Xu Q., Abo Salem H. M., Yao Y., Lou J., Huang X. The neuronal correlates of mirror therapy: a functional magnetic resonance imaging study on mirror-induced visual illusions of ankle movements. Brain Research. 2016;1639:186–193. doi: 10.1016/j.brainres.2016.03.002.
    1. Kim J., Lee B., Lee H. S., Shin K. H., Kim M. J., Son E. Differences in brain waves of normal persons and stroke patients during action observation and motor imagery. Journal of Physical Therapy Science. 2014;26(2):215–218. doi: 10.1589/jpts.26.215.
    1. Kim J. H., Lee B. H. Action observation training for functional activities after stroke: a pilot randomized controlled trial. NeuroRehabilitation. 2013;33(4):565–574. doi: 10.3233/NRE-130991.
    1. Chang M. Y., Kim H. H., Kim K. M., Oh J. S., Jang C., Yoon T. H. Effects of observation of hand movements reflected in a mirror on cortical activation in patients with stroke. Journal of Physical Therapy Science. 2017;29(1):38–42. doi: 10.1589/jpts.29.38.
    1. Martin M., Nitschke K., Beume L., et al. Brain activity underlying tool-related and imitative skills after major left hemisphere stroke. Brain. 2016;139(5):1497–1516. doi: 10.1093/brain/aww035.
    1. Bae S. H., Jeong W. S., Kim K. Y. Effects of mirror therapy on subacute stroke patients’ brain waves and upper extremity functions. Journal of Physical Therapy Science. 2012;24(11):1119–1122. doi: 10.1589/jpts.24.1119.
    1. Bhasin A., Bhatia R., Kumaran S. S., Mohanty S., Padma Srivastava M. V. Neural interface of mirror therapy in chronic stroke patients: a functional magnetic resonance imaging study. Neurology India. 2012;60(6):570–576. doi: 10.4103/0028-3886.105188.
    1. Brunner I. C., Skouen J. S., Ersland L., Gruner R. Plasticity and response to action observation: a longitudinal fMRI study of potential mirror neurons in patients with subacute stroke. Neurorehabilitation and Neural Repair. 2014;28(9):874–884. doi: 10.1177/1545968314527350.
    1. Dettmers C., Nedelko V., Ariel Schoenfeld M. Impact of left versus right hemisphere subcortical stroke on the neural processing of action observation and imagery. Restorative Neurology and Neuroscience. 2015;33(5):701–712. doi: 10.3233/RNN-140487.
    1. Frenkel-Toledo S., Bentin S., Perry A., Liebermann D. G., Soroker N. Mirror-neuron system recruitment by action observation: effects of focal brain damage on mu suppression. NeuroImage. 2014;87:127–137. doi: 10.1016/j.neuroimage.2013.10.019.
    1. Garrison K. A., Aziz-Zadeh L., Wong S. W., Liew S. L., Winstein C. J. Modulating the motor system by action observation after stroke. Stroke. 2013;44(8):2247–2253. doi: 10.1161/STROKEAHA.113.001105.
    1. Kuk E. J., Kim J. M., Oh D. W., Hwang H. J. Effects of action observation therapy on hand dexterity and EEG-based cortical activation patterns in patients with post-stroke hemiparesis. Topics in Stroke Rehabilitation. 2016;23(5):318–325. doi: 10.1080/10749357.2016.1157972.
    1. Michielsen M. E., Selles R. W., van der Geest J. N., et al. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabilitation and Neural Repair. 2011;25(3):223–233. doi: 10.1177/1545968310385127.
    1. Michielsen M. E., Smits M., Ribbers G. M., et al. The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. Journal of Neurology, Neurosurgery & Psychiatry. 2011;82(4):393–398. doi: 10.1136/jnnp.2009.194134.
    1. Rossiter H. E., Borrelli M. R., Borchert R. J., Bradbury D., Ward N. S. Cortical mechanisms of mirror therapy after stroke. Neurorehabilitation and Neural Repair. 2015;29(5):444–452. doi: 10.1177/1545968314554622.
    1. Saleh S., Adamovich S. V., Tunik E. Mirrored feedback in chronic stroke: recruitment and effective connectivity of ipsilesional sensorimotor networks. Neurorehabilitation and Neural Repair. 2014;28(4):344–354. doi: 10.1177/1545968313513074.
    1. Szameitat A. J., Shen S., Conforto A., Sterr A. Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients. NeuroImage. 2012;62(1):266–280. doi: 10.1016/j.neuroimage.2012.05.009.
    1. Wang J., Fritzsch C., Bernarding J., et al. Cerebral activation evoked by the mirror illusion of the hand in stroke patients compared to normal subjects. NeuroRehabilitation. 2013;33(4):593–603. doi: 10.3233/NRE-130999.
    1. Tani M., Ono Y., Matsubara M., et al. Action observation facilitates motor cortical activity in patients with stroke and hemiplegia. Neuroscience Research. 2017 doi: 10.1016/j.neures.2017.10.002.
    1. Brunetti M., Morkisch N., Fritzsch C., et al. Potential determinants of efficacy of mirror therapy in stroke patients – a pilot study. Restorative Neurology and Neuroscience. 2015;33(4):421–434. doi: 10.3233/RNN-140421.
    1. Marque P., Gasq D., Castel-Lacanal E., De Boissezon X., Loubinoux I. Post-stroke hemiplegia rehabilitation: evolution of the concepts. Annals of Physical and Rehabilitation Medicine. 2014;57(8):520–529. doi: 10.1016/j.rehab.2014.08.004.
    1. Askim T., Indredavik B., Vangberg T., Haberg A. Motor network changes associated with successful motor skill relearning after acute ischemic stroke: a longitudinal functional magnetic resonance imaging study. Neurorehabilitation and Neural Repair. 2009;23(3):295–304. doi: 10.1177/1545968308322840.
    1. Nowak D. A., Grefkes C., Ameli M., Fink G. R. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabilitation and Neural Repair. 2009;23(7):641–656. doi: 10.1177/1545968309336661.
    1. Small S. L., Buccino G., Solodkin A. Brain repair after stroke—a novel neurological model. Nature Reviews Neurology. 2013;9(12):698–707. doi: 10.1038/nrneurol.2013.222.
    1. Koski L., Wohlschläger A., Bekkering H., et al. Modulation of motor and premotor activity during imitation of target-directed actions. Cerebral Cortex. 2002;12(8):847–855. doi: 10.1093/cercor/12.8.847.
    1. Liew S. L., Garrison K. A., Werner J., Aziz-Zadeh L. The mirror neuron system: innovations and implications for occupational therapy. OTJR: Occupation, Participation and Health. 2012;32(3):79–86. doi: 10.3928/15394492-20111209-01.
    1. Newman-Norlund R., van Schie H. T., van Hoek M. E. C., Cuijpers R. H., Bekkering H. The role of inferior frontal and parietal areas in differentiating meaningful and meaningless object-directed actions. Brain Research. 2010;1315:63–74. doi: 10.1016/j.brainres.2009.11.065.
    1. Hamzei F., Lappchen C. H., Glauche V., Mader I., Rijntjes M., Weiller C. Functional plasticity induced by mirror training: the mirror as the element connecting both hands to one hemisphere. Neurorehabilitation and Neural Repair. 2012;26(5):484–496. doi: 10.1177/1545968311427917.
    1. Kang Y., Park H., Kim H., et al. Upper extremity rehabilitation of stroke: facilitation of corticospinal excitability using virtual mirror paradigm. Journal of NeuroEngineering and Rehabilitation. 2012;9(1):p. 71. doi: 10.1186/1743-0003-9-71.
    1. Shih T. Y., Wu C. Y., Lin K. C., et al. Effects of action observation therapy and mirror therapy after stroke on rehabilitation outcomes and neural mechanisms by MEG: study protocol for a randomized controlled trial. Trials. 2017;18(1):p. 459. doi: 10.1186/s13063-017-2205-z.
    1. Fogassi L., Ferrari P. F., Gesierich B., Rozzi S., Chersi F., Rizzolatti G. Parietal lobe: from action organization to intention understanding. Science. 2005;308(5722):662–667. doi: 10.1126/science.1106138.
    1. Giaquinto S., Cobianchi A., Macera F., Nolfe G. EEG recordings in the course of recovery from stroke. Stroke. 1994;25(11):2204–2209. doi: 10.1161/01.STR.25.11.2204.
    1. Neuper C., Wortz M., Pfurtscheller G. ERD/ERS patterns reflecting sensorimotor activation and deactivation. Progress in Brain Research. 2006;159:211–222. doi: 10.1016/S0079-6123(06)59014-4.
    1. Fox N. A., Bakermans-Kranenburg M. J., Yoo K. H., et al. Assessing human mirror activity with EEG mu rhythm: a meta-analysis. Psychological Bulletin. 2016;142(3):291–313. doi: 10.1037/bul0000031.
    1. Hobson H. M., Bishop D. V. M. The interpretation of mu suppression as an index of mirror neuron activity: past, present and future. Royal Society Open Science. 2017;4(3, article 160662) doi: 10.1098/rsos.160662.
    1. Rizzolatti G., Cattaneo L., Fabbri-Destro M., Rozzi S. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiological Reviews. 2014;94(2):655–706. doi: 10.1152/physrev.00009.2013.
    1. Babiloni C., del Percio C., Vecchio F., et al. Alpha, beta and gamma electrocorticographic rhythms in somatosensory, motor, premotor and prefrontal cortical areas differ in movement execution and observation in humans. Clinical Neurophysiology. 2016;127(1):641–654. doi: 10.1016/j.clinph.2015.04.068.

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